Charles J. Krebs

Population Cycles in Small Mammals

Publisher Summary This chapter summarizes the current information on population cycles in small rodents. It first looks at the general questions about cycles, and then discusses the demographic machinery which drives the changes in numbers. And finally, analyzes the current theories which explain population cycles in rodents. Population cycles in voles and lemmings are accompanied by a series of changes. A few of them include fluctuations occurring in a variety of genera and species from arctic to temperate areas, from Mediterranean to continental climates, from snowy areas to snow-free areas. Populations living in a wide variety of plant communities in a small geographic area all fluctuate in the same way, often in phase. Survival of adult males fluctuates independently of that of adult females, when viewed on a weekly time scale. Males may suffer heavy losses in the decline for a few weeks when females are surviving very well, and vice versa.

Impact of food and predation on the snowshoe hare cycle.

Snowshoe hare populations in the boreal forests of North America go through 10-year cycles. Supplemental food and mammalian predator abundance were manipulated in a factorial design on 1-square-kilometer areas for 8 years in the Yukon. Two blocks of forest were fertilized to test for nutrient effects. Predator exclosure doubled and food addition tripled hare density during the cyclic peak and decline. Predator exclosure combined with food addition increased density 11-fold. Added nutrients increased plant growth but not hare density. Food and predation together had a more than additive effect, which suggests that a three-trophic-level interaction generates hare cycles.

Microtus Population Biology: Demographic Changes in Fluctuating Populations of M. Ochrogaster and M. Pennsylvanicus in Southern Indiana

Microtus pennsylvanicus and M. ochrogaster are sympatric in southern Indiana grasslands. From June 1965 to August 1967 four populations were lived trapped, three of them in 0.8—hectare (2—acre) outdoor pens. Both species increased during 1965 and reached peak densities in summer 1966. Microtus ochrogaster declined abruptly that fall and remained low; M. pennsylvanicus declined the following spring. One of the fenced populations increased to a density about three times that of its unfenced control. By early fall 1966 it had nearly destroyed its food resources and then suffered a severe decline associated with obvious overgrazing and starvation. No such overgrazing has been seen on any unfenced grasslands in this area. Dispersal is probably necessary for normal population regulation in these voles, since fenced populations seem unable to regulate their density below the limit set by starvation. Both species bred extensively in the winter of 1965—66 during the phase of population increase. There was little or no breeding during the winter after the peak. Survival of females in the trappable population of both species was high and relatively constant until the end of the cycle. In males, periods of low survival punctuated the increase and peak phases, and these periods of low male survival did not occur at the same time in the two Microtus species. Some mortality processes are thus highly specific for sex and species. In the fenced populations survival rates were very high and no sporadic male losses occurred. Increasing and peak populations of M. pennsylvanicus and M. ochrogaster are characterized by adults of large body size. During the increase and peak phases some voles stopped growing at low weights (30—40 g) while others reached high asymptotic weights (45—55 g). The demography of these Microtus species in southern Indiana is similar to that of other cycle voles and lemmings in temperate and arctic areas.

Population Cycles Revisited

Periodic fluctuations or cycles in populations of small mammals have been widely studied, but much controversy still exists about their causes. Cycles of voles and lemmings are produced by the integrated effects of intrinsic and extrinsic factors, and the problem is to define accurately how these interact. Spacing behavior is a key component of population regulation in voles and lemmings, and this is illustrated most dramatically by the fence effect. We do not know which mechanisms produce changes in social behavior. Phenotypic changes produced by maternal effects or stress are now believed most likely, but there has been too little work done on genetic effects on spacing and we know almost nothing about kin-related social behavior in voles and lemmings. Both predation and food supply may be the extrinsic factors involved in cyclic population dynamics. Single-factor experiments suggest that food shortage by itself does not seem to be a necessary factor for cycles nor does predation, but the interaction between food and predation could be a key variable in understanding how extrinsic factors affect cycles of voles. Cycles of snowshoe hares are caused by an interaction between predation and food supplies, possibly integrated through risk-sensitive foraging. Spacing behavior is not a component of cycles of hares because snowshoe hares differ from voles and lemmings in having no known form of spacing behavior that can produce social mortality. The short-term cycle of voles and lemmings thus seems to have a different explanation from the long-term cycle of snowshoe hares. In some places, lemmings may be locked in a predator-pit at low density. Experimental exclusion of predators improved survival of adults in a population of collared lemmings, but was not sufficient to allow them to escape the predator-pit because of losses of juveniles. Whether cyclic populations of lemmings also fall into a predator-pit in the low phase remains to be determined. The low phase does not occur in every cycle and it is particularly difficult to explain. Progress in analyzing cyclic fluctuations has been made most rapidly when we define clear alternative hypotheses and carry out experimental manipulations on field populations. Much remains to be done on these small mammals.

The sensitive hare: sublethal effects of predator stress on reproduction in snowshoe hares

1. Prey responses to high predation risk can be morphological or behavioural and ultimately come at the cost of survival, growth, body condition, or reproduction. These sub-lethal predator effects have been shown to be mediated by physiological stress. We tested the hypothesis that elevated glucocorticoid concentrations directly cause a decline in reproduction in individual free-ranging female snowshoe hares, Lepus americanus. We measured the cortisol concentration from each dam (using a faecal analysis enzyme immunoassay) and her reproductive output (litter size, offspring birth mass, offspring right hind foot (RHF) length) 30 h after birth. 2. In a natural monitoring study, we monitored hares during the first and second litter from the population peak (2006) to the second year of the decline (2008). We found that faecal cortisol metabolite (FCM) concentration in dams decreased 52% from the first to the second litter. From the first to the second litter, litter size increased 122%, offspring body mass increased 130%, and offspring RHF length increased 112%. Dam FCM concentrations were inversely related to litter size (r(2) = 0.19), to offspring birth mass (r(2) = 0.32), and to offspring RHF length (r(2) = 0.64). 3. In an experimental manipulation, we assigned wild-caught, pregnant hares to a control and a stressed group and held them in pens. Hares in the stressed group were exposed to a dog 1-2 min every other day before parturition to simulate high predation risk. At parturition, unsuccessful-stressed dams (those that failed to give birth to live young) and stressed dams had 837% and 214%, respectively, higher FCM concentrations than control dams. Of those females that gave birth, litter size was similar between control and stressed dams. However, offspring from stressed dams were 37% lighter and 16% smaller than offspring from control dams. Increasing FCM concentration in dams caused the decline of offspring body mass (r(2) = 0.57) and RHF (r(2) = 0.52). 4. This is the first study in a free-ranging population of mammals to show that elevated, predator-induced, glucocorticoid concentrations in individual dams caused a decline in their reproductive output measured both by number and quality of offspring. Thus, we provide evidence that any stressor, not just predation, which increases glucocorticoid concentrations will result in a decrease in reproductive output.

Predation and Population Cycles of Small Mammals A reassessment of the predation hypothesis

The periodicity of mass occurrence of some northern small rodents has been known from at least the mid-sixteenth century, when Archbishop of Uppsala, Sweden, Olaus Magnus, published two reports on the phenomenon. He suggested that lemming abundances peaked at intervals of approximately three years (Stenseth and Ims 1993a). Elton (1942) initiated research on periodic fluctuations in small mammal populations, and since then such fluctuations have been the focus of much research and controversy in animal ecology. Cyclic fluctuations of population densities of many northern mammals are characterized by a regular period (the interval between successive density peaks) and a highly variable amplitude (the ratio of maximum to minimum population density). In the boreal zone of North America and some parts of Siberia, the cycle period is usually 9-10 (811) years, and the cycle amplitude

What Drives the 10-year Cycle of Snowshoe Hares?

n 1831 the manager of a Hudson’s Bay Company post in northern Ontario wrote to the head office in London. The local Ojibway Indians were starving, he reported, because of a scarcity of “rabbits,” and they were unable to trap for furs because they spent all their time fishing for food (Winterhalder 1980). These shortages of so-called rabbits, which apparently occurred approximately every 10 years, are regularly mentioned in Canadian historical documents from the 18th and 19th centuries. Those rabbits were in fact snowshoe hares (Lepus americanus), and their 10-year cycle is one of the most intriguing features of the ecology of the boreal forest. Ten-year cycles were first analyzed quantitatively when wildlife biologists began to plot the fur trading records of Hudson’s Bay Company during the early 1900s. The Hudson’s Bay Company, established in 1671, kept meticulous records of the numbers of furs traded from different posts spread across Canada. The most famous time series drawn together from those records was that of Canada lynx (Elton and Nicholson 1942; Figure 1). The lynx is a specialist predator of snowshoe hares, and the rise and fall in lynx numbers mirrors, with a slight time lag, the rise and fall of snowshoe hare populations across the boreal region. The spectacular cycles of snowshoe hares and their predators have captured the attention of biologists as well as historians. These cycles are highlighted in virtually all ecology texts and are often cited as one of the few examples of Lotka-Volterra predator‐prey equations, a simple model which shows never-ending oscillations in the numbers of predators and their prey. Cycles seem to violate the implicit assumption of many ecologists that there is a balance in nature, and anyone living in the boreal forest would be hard pressed to recognize a balance among the boom and bust in nature’s economy. The challenge to biologists has been to understand the mechanisms behind these cycles, which has not been easy. One cycle lasts 10 years, and few PhD students or researchers wish to take 10 years to obtain n = 1. Fortunately,

Genetic, Behavioral, and Reproductive Attributes of Dispersing Field Voles Microtus pennsylvanicus and Microtus ochrogaster

To investigate experimentally the relationship between dispersal and population regulation in small mammals, voles were removed continuously from two plots in southern Indiana for 2 years. Three control populations of two Microtus species were monitored over the same period, and animals dispersing onto the experimental areas were compared with resident control animals for the following characteristics: (1) age, weight, and sex; (2) genotype for two polymorphic plasma proteins, leucine aminopeptidase (LAP) and transferrin (Tf); and (3) exploratory, aggressive, and general activity behavior of males. Dispersal was most common during the fall and winter, and in the phase of population increase 59% of male and 69% of female Microtus pennsylvanicus loss from two control populations could be accounted for by dispersal. In contrast, little of the high loss during the population decline could be associated with dispersal. In the late peak and decline periods male M. pennsylvanicus of the Tf—E and LAP—S phenotypes...

FUNCTIONAL RESPONSES OF COYOTES AND LYNX TO THE SNOWSHOE HARE CYCLE

Coyotes and lynx are the two most important mammalian predators of snow- shoe hares throughout much of the boreal forest. Populations of hares cycle in abundance, with peaks in density occurring every 8-11 yr, and experimental results suggest that pre- dation is a necessary factor causing these cycles. We measured the functional responses of coyotes and lynx during a cyclic fluctuation of hare populations in the southwest Yukon, to determine their effect on the cyclic dynamics. We used snow-tracking and radio telemetry to examine changes in the foraging behavior of the predators. Coyotes and lynx both fed mostly on hares during all winters except during cyclic lows, when the main alternative prey of coyotes was voles, and lynx switched to hunting red squirrels. Both predators showed clear functional responses to changes in the densities of hares. Kill rates of hares by coyotes varied from 0.3 to 2.3 hares/d, with the most hares killed one year before the cyclic peak, while those of lynx varied from 0.3 to 1.2 hares/d, with the highest one year after the peak. Maximum kill rates by both predators were greater than their energetic needs. The functional response of coyotes was equally well described by linear and type-2 curves, and that of lynx was well described by a type-2 curve. Kill rates by coyotes were higher during the increase in density of hares than during the cyclic decline, while the reverse was true for lynx. Coyotes killed more hares early in the winter, and cached many of these for later retrieval. Lower densities of hares were associated with longer reactive distances of both predators to hares, but with little apparent change in time spent searching or handling prey. In summary, our data show that the two similarly sized predators differed in their foraging behavior and relative abilities at capturing alternative prey, leading to different patterns in their functional responses to fluctuations in the density of their preferred prey.

Newly discovered landscape traps produce regime shifts in wet forests

We describe the “landscape trap” concept, whereby entire landscapes are shifted into, and then maintained (trapped) in, a highly compromised structural and functional state as the result of multiple temporal and spatial feedbacks between human and natural disturbance regimes. The landscape trap concept builds on ideas like stable alternative states and other relevant concepts, but it substantively expands the conceptual thinking in a number of unique ways. In this paper, we (i) review the literature to develop the concept of landscape traps, including their general features; (ii) provide a case study as an example of a landscape trap from the mountain ash (Eucalyptus regnans) forests of southeastern Australia; (iii) suggest how landscape traps can be detected before they are irrevocably established; and (iv) present evidence of the generality of landscape traps in different ecosystems worldwide.